The paper makes some pretty hefty claims regarding dinosaur metabolism, and as such, has received a fairshare of media coverage touting this as the latest evidence for “warm-blooded” (i.e., automatic endothermic) dinosaurs.
Every time there is a major headline like that, I feel obliged to go back to the source to see what the media has likely overblown. In this case, media claims don’t seem that far off what was written in the actual paper, which is not necessarily good. Some of these claims do extend beyond the reach of the available evidence (e.g., there actually is no comparison with other contemporaneous reptiles of the region, weakening any arguments for metabolic thermoregulation).
It’s been an age since I’ve done one of these paper breakdowns, but I think this one warrants a more thorough analysis, especially given the implications of the interpretations.
In another example of slow-cooked science, this paper was the culmination of over three years worth of work collecting data on tegus. For the study, the authors looked at adult black and white tegus (Salvatore merianae). Tegus are an interesting group of lizards. They are the largest members of the family Teiidae and are often referred to as the monitor lizards of the new world, due to their convergent lifestyles (highly predaceous, active foragers). Besides their varanid-like demeanor, tegus are also known for their enormous jowls, especially in the males. The jowls hold the pterygoideus muscles, the big jaw snappers, which have been shown to increase in size for males during the breeding season (Naretto et al. 2014). As reptiles, tegus have been assumed to follow the standard ectothermic lifestyle of requiring external sources of heat to warm their bodies and maintain stable body temperatures. Looking at the natural history of the animals, tegus appear to fit the mold pretty well. They have distinctive winter and summer activity levels. In the summer, the animals regularly maintained body temperatures of 32â€“35Â°C, and in the winter they let their body temperatures drop to the temperature of their burrows (15â€“20Â°C). This is all fine and good for a bradymetabolic, ectothermic lizard, but when the researchers tracked body temperatures over time they discovered something completely unexpected.
This year has seen the discovery of two big deal dinosaur specimens. At least they are a big deal in regards to dinosaur integument and, possibly, metabolism.
First off from a few months ago we had the announcement the theropodÂ Yutyrannus hauli, the “beautiful feathered tyrant.”
Xu, X., Kebai, W., Ke, Z., Qingyu, M., Lida, X., Sullivan, C., Dongyu, H., Shuqing, C., Shuo, W. 2012. A Gigantic Feathered Dinosaur from the Lower Cretaceous of China. Nature. Vol.484:92-95
This was not just a single fossil, but a collection of three fossils (one might be tempted to call it a family group, but that would only be speculation). As with all other dinosaur fossils that have been found to have filamentous integument, these guys come from Liaoning, China. They are suspected to have come from the Jehol Group in the Yixian formation. I say suspected because the complete three specimen set was a purchase from a fossil dealer, an all too common occurrence for Chinese fossils. As such the provenance information is unknown. A lot of Chinese fossil dealers don’t like to give away the location of their find due to the potential loss of other profitable specimens. This current trend in China is a good example of what happens when capitalism comes into play with fossil collecting (something that the U.S. has been mostly, but not entirely, able to avoid). So it is currently uncertain whether these fossils are from the Yixian. However given that all the others guys are too it is probably a good bet. Given the sketchy nature in which many Yixian fossils are collected, coupled with the possibly large consequences of the find, one should naturally be skeptical of the fossil. Had it been one individual on multiple slabs I would question its validity as a real thing. However since Y.huali is known from three individuals, and the filaments seem to follow a consistent pattern around the body (compare that to the helter-skelter nature of Tianyulong‘s preservation), forgery seems unlikely. These guys are probably the real deal. This has some potentially far reaching consequences to interpretations of Late Cretaceous coelurosaurs and the Jehol Biota itself (more on this in a bit).
The second announcement came just a few weeks ago. This was the discovery of a potentially new, miniscule theropod from Bavaria Germany.
Rauhut, O.W.M., Foth, C., Tischlinger, H., Norell, M.A. 2012. Exceptionally Preserved Juvenile Megalosauroid Theropod Dinosaur with Filamentous Integument from the Late Jurassic of Germany. PNAS Early Edition:1203238109v1-201203238.
The specimen is exceptionally well preserved. So well preserved in fact that it actually looks like a plastic toy. While this degree of preservation warrants importance all its own, the main interest behind this new guyâ€”dubbed: Sciurumimusalbersdoerferi (AlbersdÃ¶rfer’s squirrel mimic)â€”is the apparent presence of filamentous integument on the body coupled with its apparent placement among much more basal theropods. This discovery has far reaching consequences for theropod integument interpretations. Note: As with Y.hauli, Sciurumimusalbersdoerferiwas also purchased from a private collector. I don’t suspect forgery here either as this was in Germany, where fossil dealing is neither a big problem nor a lucrative business. The exceptional detail on the specimen would also require a substantial amount of theropod knowledge to pull off. Anyone having that amount of knowledge is more likely to be a real paleontologist than a get rich quick forger.
Last timeI gave a brief (?) run through the various types of metabolic rates that we find in the animal kingdom, along with the various ways in which they were measured. There was one last metabolic rate type I wanted to cover, but instead only teased; that of mass specific metabolic rate (MSMR). This type of metabolic rate measurement is fundamentally different from all the others that we talked about previously, and coupled with the sordid history behind this concept, it seemed appropriate to give MSMR its own post.
So without further ado, let’s get this party started.
MSMR = Mass Specific Metabolic Rate
Dinosaur fanatics will no doubt recognize this infamous phrase. It tends to pop up a lot in literature dealing with dinosaur energetics. Mass specific metabolic rate differs from other MR measurements because it is not an actual measurement. Rather, MSMR is a mathematical abstraction taken from actual metabolic rate measurements of multiple taxa spanning a wide range of sizes. Ultimately what MSMR does is show us how metabolism scales with size. That in itself deserves a brief digression.
Scaling and biology
Size can radically change an organism’s structure, and function. The reasons for this relate back to some fundamental physical properties of all things. For instance, consider the metrics of height, width and length. Each of these measurements, taken by themselves, represent one dimension only. If one wants to get the idea of the size of a two dimensional object, one need only combine (multiply) any two of these measurements. If we combine all three we can get a good 3-D representation of how much space an object takes up.
If any structure is to grow isometrically (i.e. everything grows at the same rate) then for any increase in a linear measurement (length, width, or height) the area of that object will double, while the volume of the object will triple.
For instance, if an object that was 1 meter long, suddenly doubled in size isometrically, its area would increase by:
2m x 2m = 2m2, or 4 meters in area (4 square meters).
While the object doubled its length, it quadrupled its area.
Meanwhile the volume of that object will increase by a multiple of all three linear measurements:
2m x 2m x 2m, = 2m3, or 8 meters in volume/mass (8 cubic meters).
So now the object that has increased its linear measurements by 2, increased its surface area by 4 and increased its mass by 8.
This has immediate implications for any organism. If we look at just vertebrates we find that the strength of things such as bone and muscle are determined by their cross sectional area.
To put this in more practical terms: for any given change in length, width or height of an isometrically growing organism, strength is going to double while weight is going to triple. The obvious problem here being that eventually (and rather quickly) weight is going to outpace strength. This puts a limit on how big an organism can get. It also explains why the short guy in gym class can always do more chin ups than the taller guys.
The way that life has found around this isometry problem is to just dump the concept of isometry altogether. Instead, organisms will grow different body parts at accelerated, or decelerated rates (e.g. increasing bone density and muscle size faster than other organs for large animals). This is referred to as allometry. In general, allometric equations are generally some type of variable regressed against body mass. By doing so, one is able to determine how that variable is changing in relation to a change in size. It tends to look something like this:
y = aMbb
Where a is an experimentally determined allometric coefficient, Mb is body mass, and b is the allometric exponent.
For the purposes of this discussion the general rule is that bigger vertebrates will have relatively bigger bones and muscles than a smaller vertebrates scaled up to their size.
Rubner, Kleiber and metabolic scaling: battle of the Maxes.
If bigger creatures generally show an allometric increase in size for various body parts, then one would expect to find some kind of similar allometric effect for metabolism. After all, a bigger animal is going to be composed of more cells, which will require more energy to power. So then should we expect metabolic rate to scale to mass (i.e. to increase by the third power?). Perhaps, but one should also keep in mind that as each of these cells expends energy, they are also producing a little bit of heat. Thus more cells results in a hotter critter. In animals, heat is lost primarily via conduction; a process that is intimately associated with surface area. Perhaps, then, it would be better if metabolic rate followed surface area instead, and increased by the second power.
However which way metabolism scales it looks like it should relate somehow to these two variables.
In order to figure this out, one must measure the lowest metabolic rate of one’s animals — the BMR/SMR. The reason for using BMR/SMR is that one is theoretically looking at the “metabolic floor.,” or the MR level that must be maintained to avoid death (and, thus the MR that is not likely to be affected by food acquisition, exercise, stress, etc.). The importance of using BMR will come up again further down.
One measures the BMR/SMR of one’s animals and plots those metabolic rates against the size of the animals measured. From this one should be able to acquire a ratio of metabolic rate to mass. Often the data must be regressed first in order to achieve any kind of statistical analysis.
The first attempts at this were done using mammals, and one of the most influential people to try this out was Max Rubner. Rubner measured the metabolic rate of dogs and regressed these data against mass. What he found was that as body size increased, metabolic rate increased by approximately 2.325 times. Rubner took this one step further and found that his exponent for metabolic rate could be made mass independent by simply subtracting it from the exponent for mass (3.0). The end result: mass specific metabolic rate for dogs appeared to increase by the 0.675 power, or the 2/3rds power (Rubner 1883).
So what does all of this mean? Essentially it means that metabolism increases slower than body mass. So if we were to graph out metabolism in relation to the amount of mass that that metabolism is powering, we would discover that the data form a negative slope, with bigger animals falling further towards the low end of the slope than smaller animals. To put it more succinctly, it takes less relative metabolic energy to power a larger mass than it does to power a smaller mass. This is mass specific metabolism.
A common misconception about MSMR is that metabolic rate goes down as one gets larger, but this is not the case at all. The metabolism of a large animal is still larger than that of a small animal, it is just that for a given mass, the increase in metabolism is less than one would expect. For example if you took the BMR of a large beagle (14kg) and the BMR of a boxer (30kg), one would expect the boxer to show a basal metabolic rate that is at least twice as fast as that of the beagle (since it is roughly twice the mass of the beagle). If we input the data into the allometric equation mentioned earlier, we get:
*The 89kcal/day/kg is the allometric constant given by Rubner 1883. It is the average BMR for his dogs after correcting for mass.
What we find is that the boxer does have a higher metabolic rate than the beagle, but it is only 1.67 times greater, instead of 2. This lower than expected metabolic rate will translate to lower than expected food costs as well. To put it another way: it would be cheaper to feed one boxer than to feed two beagles of roughly the same size, or to shift things away from dogs: it is cheaper to feed one elephant than it is to feed an elephant’s weight in shrews.
Rubner’s discovery was amazing and his equation elegant. It became to be referred to as: Rubner’s surface law of metabolism; a law that would stay in practice for 50 years afterward. It wasn’t until 1932 that this law was officially challenged, and by another Max at that. Swiss agricultural chemist Max Kleiber studied MSMR in mammals ranging from rats to cows. He plotted their body masses and BMRs on a logarithmic scale, and came to the conclusion that Rubner’s 2/3rd surface area law was incorrect. Rather mass-specific metabolism followed a “higher power.” That of 3/4, or 0.75. It’s interesting to note that the result Kleiber found was in fact not quite 0.75 (it was 0.73). This number was rounded to 0.75 in order to make it more “slide rule friendly” (Schmidt-Nielsen 1984)
Quarter power laws for everyone.
So Rubner’s law was broken, and Kleiber’s law came in to replace it. For over 70 years Kleiber’s law was held up as that rare case of a biological constant Subsequent BMR studies of mammals (Brody 1945) and other organisms including bacteria (Hemmingsen 1960) found results that “hovered” around 0.75, thus suggesting that this biological law was not just a mammal thing, but rather a hallmark of all organisms.
This leads us to the obvious question of why?
Typically, the response to this question is a thermal one. Small animals lose heat easier than large animals, due to their larger relative surface area. If a large animal has an easier time retaining body heat, then it would make sense that its body would need to produce relatively less of it. The problem with this answer is that it only works for automatic endotherms (i.e. mammals and birds). However the MSMR phenomenon is present in bradymetabolic thermoconformers too. Therefore this answer cannot be the only one.
The answer to this question had remained elusive up until 14 years ago, when West et al proposed that the quarter power scaling laws that we see in nature appear to be the result of the fractal nature of delivery networks (West et al 1997), which in the case of vertebrates, are blood vessels. West et al. proposed that the fractal nature of blood vessels, combined with area preserving branching patterns could be used to explain why metabolism scales to the 3/4 power. The work by West et al was the first real attempt to explain why metabolism should scale to the 3/4 power, and has since been referred to as the metabolic theory of ecology.
Data on MSMR calculations from Brody and Hemmingsen all seemed to show that everything followed the 3/4 exponent rule. These two papers, along with Kleiber’s influential work, are some of the most cited papers in the physiological literature. One the one hand this illustrates just how influential their findings were for biology in general, but on the other hand it also suggests that their work should be the most thoroughly scrutinized. Scientists occasionally take the work of others for granted. This can lead to unpleasant side effects and near dogmatic views of things (e.g. the old saw about swamp bound dinosaurs). In general, it is a good idea to occasionally go back to these seminal works and verify that the authors got things right the first time.
Dodds et al. (2001) did just that. The authors looked back at the work of Brody, Hemmingsen, Keliber and others in the field of MSMR, in order to see if the 3/4 power law was a real thing, or mathematical error. Their results found that data from as far back as 1982 suggested that there was a problem with the 3/4 power law. Much of the data that had come out since Kleiber, Brody and Hemmingsen’s time suggested that the exponent for metabolic power should lie much closer to 2/3rds than 3/4. Dodds et al. went even further and challenged the metabolic theory of ecology by citing apparent mathematical errors in the work by West et al. in 1997. This challenge to the model by West et al. remains controversial, with arguments that continue to sling back and forth (e.g. Kozlowski and Konarzewski 2004, Brown et al 2005). Dodds et al (2010) recently took on the nutrient supply approach spearheaded by West et al, but looked at it from a purely geometric point of view (rather than fractal.). Their results found strong support for nutrient networks being the limiting factor for metabolic rate. Their results also found that these structures scaled to the 2/3rd power.
Kleiber’s faux pas; or: why MR type matters.
In 2003, White and Seymour gave a critical re-evaluation of Kleiber’s initial work. Kleiber was an agriculturist, and at least part of his impetus for looking at MSMR was to produce a greater yield in biomass, for farm animals. It is no surprise, then, that most of Kleiber’s study animals were of the barnyard variety. The problem with using livestock to determine MSMR is that domestic animals — especially ones that are raised for food — have been under extensive selection to produce larger animals for less cost. Thus, they are unlikely to be accurate representatives of a “wildtype” metabolic rate. Another, much larger, problem was the over-representation of artiodactyls in Kleiber’s study. In fact, both Kleiber, and Brody (and by extension Hemmingsen, as he re-used most of Brody’s data) had artiodactyls encompassing over 20% of their data.
Okay, so what exactly is the problem here?
The problem is that artiodactyls only make up approximately 5% of all extant mammals. To increase this representation by 4 times is going to skew the results. Also, as White and Seymour pointed out (2003), many of these animals were on the upper edge of the regression line, resulting in a disproportionate influence over the scaling exponent.
Topping it all off was the biggest issue of all, and one that crops up time and time again with many metabolic studies. As mentioned in part 1 of this series, BMR and RMR are not the same thing. If one is going to measure the mass specific metabolism of an animal, one must get it from the basal metabolic rate. There are strict methods for acquiring these data (McNab 1997), not the least of which is the necessity of measuring the metabolism of an animal that is in a post-absorptive state. This is a time in between eating and fasting, where the body is not doing any digestion at all. This is important because digestion can actually ramp up basal/standard metabolism substantially over resting/fasting levels. Perhaps the most dramatic example of this would be data from Burmese pythons (Python molurus) in which feeding metabolism increases SMR by over 44 times the resting rate (Secor and Diamond 1996)!
Ensuring that an animal is in a postabsorptive state is no easy task. Some taxa, such as very small mammals (e.g. shrews, hamsters, etc) run so close to the thermal edge that it might be impossible to get them in a postabsorptive state without killing them. As Speakman et al (1993) wittingly put it: “Before small shrews become post-absorptive they enter a state of profound rest in which they have zero metabolism and from which they never recover!” One might wonder, then, if BMR = RMR in such a situation (but see McNab 1997 for a counterpoint).
The problem with artiodactlys is that they are ruminants. That is to say they rely on bacterial degradation of cellulose in order to extract nutrients from their food. Because of this, the digestive phase for ruminants can last for a substantially long time. Typically, artiodactyls are fasted for 72 hours before having their BMR measured, yet data on digestion in ruminants suggests that they can last as long as 7 days before entering a postabsorptive state (White and Seymour 2005), if at all (McNab 1997). When this is not taken into account, one winds up measuring RMR instead of BMR, which raises the overall exponent to the mass specific metabolic rate equation.
Now, to be fair, Kleiber did note that his extensive use of artiodactyls (three cows and a sheep) could have an unwanted effect on his data if they were not being measured in a postabsorptive state. Thus, he performed an analysis with and without his ruminants. Interestingly, the results still hovered around 3/4ths (0.72-0.73). White and Seymour (2005) argued that the reason behind this still high exponent might be due to the relatively high BMRs of domestic carnivores (Kleiber used dogs) and humans. The authors later went on to show that the removal of these data points ultimately drops the exponent down to the 2/3rds that seem to be so commonplace among other metabolic studies.
Another aspect of BMR studies that tends to get overlooked when researchers attempt MSMR calculations is the need to measure animals in a thermoneutral environment. This is an environment in which the animal is not actively thermoregulating, otherwise known as the thermoneutral zone. Automatic endotherms are often lauded for their ability to maintain body temperatures regardless of the external environment. This seems to have lead to the assumption that the environmental temperature should not matter, which results in experiments that grab metabolic rate data from animals that are in fact, rather stressed (e.g. Hanski 1984, who measured “BMR” in shrews that were 7Â°C below their thermal neutral zone). White and Seymour noted that mass and body temperature showed an intimate relationship in mammals (White and Seymour 2003), and that in order to get a useful comparative estimate of BMR for mammals that encompasses the full range of masses seen in this group, BMR should be standardized to a common body temperature. This is very intriguing for White and Seymour have essentially taken BMR and converted it to SMR. As mentioned previously, automatic endotherms do not escape the Q10 effect, but instead keep it at bay by keeping their cells encased in a bubble of stable temperatures. This means that one can use Q10 values to adjust BMR to fit an appropriate “universal” temperature with which to compare taxa. That temperature turned out to be 36.2Â°C with a Q10 of 3.0.
White and Seymour discovered that when BMR was standardized to a universally comparable temperature, the mass specific exponent for metabolic rate was approximately 0.67, or 2/3rds. Even more fascinating: when data for birds are given the same rigorous treatment, they also scale to the 2/3rds power (McKechnie and Wolf 2004). So it appears that Rubner had it right all along. For seventy years we have been using a formula that suffered from some hefty methodological errors.
Well at least that’s all fixed now, right?
One power law to rule them all? Probably not.
Dodds, Rothman, Weitz (2001), White and Seymour’s (2003) works to turn over the established 3/4 power law belief in physiology did not go unquestioned Savage et al (2004) gave a particularly in depth critique of their analyses, pointing out some questionable assumptions that White and Seymour had made, as well as the disproportionate amount of data available for mammals (i.e. some genera were over-represented with multiple BMR measurements, while others might not have any data at all). This violates a fundamental assumption of practically every statistical analysis. Namely that data points are independent. Savage et al pointed out that most BMR data exists for mammals that are less than 1kg in size. This is going to bias the regression statistic (indeed, Dodds et al.  noted that the 2/3rd power only seemed effective for mammals up to about 10kg. The authors cited a lack of data for larger taxa as a likely cause of this strangeness).
Savage et al decided to repeat the statistical analyses of White and Seymour, as well as a few other authors. In the process they found various errors in each analysis that resulted in some major discrepancies (e.g. basal metabolic rates that varied over an order of magnitude for the same species in the same study, the exclusion of large chunks of Mammalia that spanned the larger size ranges, thus reducing their dataset). The authors separated their taxa into “bins” that covered various size ranges. The idea being that by separating mass into sections like this, they could turn mass into a treatment effect, which should allow the statistical analysis to better analyze the effect of BMR as described by body mass.
The result of Savage et al’s study showed that the scaling exponent for BMR to body mass was around 0.712 +/- 0.012. This new regression suggested that the “true” exponent for BMR in relation to mass, was neither 2/3rds, nor 3/4ths, but something in between. The authors noted this unexpected result, but quickly pointed out that this was for data that was heavily biased for small size (mostly rodents). This was where the “binning” idea would come into effect. By essentially forcing a uniform distribution across the mass ranges available the authors results revealed an exponent of 0.737 +/- 0.025, or an exponent that lives around 3/4ths.
The authors took this a step further by looking for exponents to describe field metabolic rate and maximal metabolic rate. Their reasoning being that these are more easily obtained measurements that have more biologically meaningful results to them. I am less confident of these results, as FMR encompasses many aspects of an organism’s lifestyle, while MMR can be difficult to fully obtain. Further, I would argue that the benefits of BMR is that they indicate what the bare minimum energy requirements of an organism should be. That has the potential to be extremely useful for paleontology. Especially if one is looking to figure out how much food (at minimum) an organism would need to eat to survive in some environment (and thus, infer something about thermophysiology).
White et al . (2006) responded back, by doing a more thorough analysis of available data. They disregarded Savage et al’s notion of mass “binning” (which was fine, as Savage et al. disregarded the need to adjust for temperature, citing negligibility of the results as the reason), and used data from 938 species ranging from 158mg (0.35 lbs) to 138kg (304 lbs), and covering every major vertebrate class. Data were only used if they fit the strict criteria for BMR mentioned previously, and each group was compared to a standard temperature (38Â°C and 20Â°C), after accounting for Q10 effects. Once again, White and Seymour found strong support for a 2/3rds exponent…for mammals and birds.
And this is where we come to the punchline in all of this. While the arguments had previously focused on automatic endotherms, data started to appear in both those groups, and (especially) the groups outside
Mammalia and Aves, that a universal metabolic exponent appeared not to exist. This was tackled more formally by White et al. (2007) who reviewed the current literature citing numerous examples where the single exponent view was not being met empirically. This was followed up by a final analysis by the authors on 127 published allometric exponents for taxa that spanned the range of animal classes. Following Felsenstein (1985) they incorporated independent contrasts to remove the effects of phylogeny (which has a tendency to screw the pooch for independence of data points) . The authors then assigned the exponents found to one of three categorical variables:
Taxonomy (Amphibia, Arthropoda, Aves, Actinopterygia/Chondrychthys [“fish”], Mammalia, Reptilia, Prokaryotes)
Thermoregulation (automatic endotherm, or bradymetabolic “ectotherm”)
Metabolic state (FMR, RMR, MMR, BMR/SMR)
Then, after assigning some fancy statistical mojo (weighted generalized mix model, for those that are into that kind of stuff), the authors found that among their three categories, only thermoregulation seemed to show any real affect on where the exponent wanted to go (i.e. it “pushed” the exponent towards some kind of “true mean”). This suggests that a true discrepancy between these modes of thermophysiology ultimately affect metabolic rate. Surprisingly, White et al’s study seemed to show that automatic endotherms converge at an exponent closer to 2/3rds, while everyone else hovers closer to 3/4ths. However there is still considerable sway around these exponents. So much so that White et al. urge researchers to do away with the 2/3rds 3/4ths argument altogether, as it has become quite apparent that choosing one, or the other is going to both bias results and obscure pertinent data. The authors do offer some alternatives that might be used such as statistics that incorporate multiple exponent models, accounting for body mass by using it as a variable in an analysis of covariance (ANCOVA) model, or just choosing the right exponent for the job (e.g. the 3/4ths exponent seems to work well for FMR of mammals, but overestimates the FMR of birds).
Where are we now?
So here we are, finally at the end of this long winded blog entry, and what do we have to show for it? Well…mostly that biological laws are so few and far between that any relationship, or phenomenon that has the audacity to be referred to as a “law” or “rule” should probably be taken with a grain of salt.
Another thing to take away from this is just how complicated metabolic physiology studies really are. They have to account for so many unexpected variables that is amazing we can say anything at all about extant animals. One thing I did not touch upon was the fact that all MSMR equations use regression as their model of choice. A severe limit to this approach (and one that is violated all the time) is that regression models can really only predict — with any certainty — the estimated MSMR of an animal that falls within the size range measured. Once one starts to extrapolate beyond the maximum, or minimum size of the available data, one is practically just speculating.
Lastly, given what little we are able to say about extant animal metabolism and its limits, just think about how much less we can confidently say about extinct taxa. This is especially true for paleontological studies that attempt to use metabolic scaling exponents to infer the possible thermophysiology of extinct organisms. Thus any study that attempts to do this kind of paleophysiology, would be best served by computing hypothetical BMR/SMRs that used a wide range of metabolic exponents.
And that, in a nutshell, is what all the fuss is about for MSMR.
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West,G.B., Brown,J.H., Enquist,B.J. 1997. A General Model for the Origin of Allometric Scaling Laws in Biology. Science. Vol.276:122-126
White, C.R., Cassey, P., Blackburn, T.M. 2007. Allometric Exponents do not Support a Universal Metabolic Allometry. Ecology. Vol.88(2):315-323
White, C. R., N. F. Phillips, and R. S. Seymour. 2006. The Scaling and Temperature Dependence of Vertebrate Metabolism. Biol.Letters Vol.2:125-127
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[Editor’s note: A response from the authors can be found here. It answers many of the questions I had about the paper, though I feel the biggest question remains open for debate. I appreciate the authors taking their time to answer my questions, and PLoS ONE for allowing this type of open communication.]
This post has taken an inordinate amount of time to write up. Mostly because it required finding enough free time to sit down and just type it out. So I apologize ahead of time for bringing up what is obviously old news, but I felt this paper was an important one to talk about, as it relied on a old, erroneous, but very pervasive, popular and rarely questioned hypothesis for how automatic endothermy (mammal and bird-style “warm-bloodedness”) evolved.
Back in November, a paper was published in the online journal: PLoS ONE. That paper was:
Using muscle force data for the hindlimbs of theropods, and applying it to a model based on Pontzer (2005, 2007), the authors were able to ascertain the approximate aerobic requirements needed for large bipedal theropods to move around. Their conclusion was that all but the smallest taxa had to have been automatic endotherms (i.e. warm-blooded).
Time to stop the ride and take a closer look at what is going on here.
In 2004, John Hutchinson – of the Royal Veterinary College, London UK – performed a mathematical study of bipedal running in extant taxa. He used inverse dynamics methods to estimate the amount of muscle that would be required for an animal to run bipedally. He then tested his models on extant animals (Basiliscus, Iguana, Alligator, Homo, Macropus, Eudromia, Gallus, Dromaius, Meleagris, and Struthio). The predictive capacity of his model proved to be remarkably substantial and stable (Hutchinson 2004a). A follow up paper in the same issue (Hutchinson 2004b) used this model to predict bipedal running ability in extinct taxa (Compsognathus, Coelophysis, Velociraptor, Dilophosaurus, Allosaurus, Tyrannosaurus and Dinornis). Results from this study echoed previous studies on the running ability of Tyrannosaurus rex (Hutchinson & Garcia 2002), as well as provided data on the speed and agility of other theropod taxa.
Meanwhile in 2005, Herman Pontzer – of Washington University in St. Louis, Missouri – did a series of experiments to determine what was ultimately responsible for the cost of transport in animals. To put it another way: Pontzer was searching for the most expensive thing animals have to pay for in order to move around. One might intuitively assume that mass is the ultimate cost of transport. The bigger one gets, the more energy it requires to move a given unit of mass, a certain distance. However experiments on animals found the opposite to be the case. It actually turns out that being bigger makes one “cheaper” to move. So then what is going on here?
Pontzer tested a variety of options for what could be happening; from extra mass, to longer strides. In the end Pontzer found that the effective limb length of animals, was ultimately the limiting factor in their locomotion. Effective limb length differs from the entirety of the limb. Humans are unique in that our graviportal stance has us using almost our entire hindlimbs. Most animals, however, use a more crouched posture that shrinks the overall excursion distance of the hindlimb (or the forelimb). By taking this into account Pontzer was able to find the one trait that seemed to track the best with cost of transport in animals over a wide taxonomic range (essentially: arthropods – birds).
This latest study combines these two technique in order to ascertain the minimum (or approx minimum) oxygen requirements bipedal dinosaurs would need in order to walk, or run.
As with the previous papers, the biomechanical modeling and mathematics are elegant and robust. However, this paper is not without its flaws. For instance in the paper the authors mention:
We focused on bipedal species, because issues of weight distribution between fore and hindlimbs make biomechanical analysis of extinct quadrupeds more difficult and speculative.
Yet this did not stop the authors from applying their work on bipeds, to predicting the maximum oxygen consumption of quadrupedal iguanas and alligators. No justification is ever really given for why the authors chose to do this. Making things even more confusing, just a few sentences later, it is mentioned (ref #s removed to avoid confusion):
Additionally, predicting total muscle volumes solely from hindlimb data for the extant quadrupeds simply assumes that the fore and hindlimbs are acting with similar mechanical advantage, activating similar volumes of muscle to produce one Newton of GRF. This assumption is supported by force-plate studies in other quadrupeds (dogs and quadrupedal chimpanzees)
The force plate work cited is for quadrupedal mammals. However, mammals are not reptiles. As Nicholas Hotton III once mentioned (1994), what works for mammals, does not necessarily work for reptiles. This is especially so for locomotion.
In many reptiles (including the taxa used in this study) the fore and hindlimbs are subequal in length; with the hindlimbs being noticeably longer and larger. Most of the propulsive power in these reptiles comes from the hindlimbs (which have the advantage of having a large tail with which to lay their powerful leg retractor on). The result is that – unlike mammals – many reptiles are “rear wheel drive.”
The last problem is by far the largest, and ultimately proves fatal to the overall conclusions of the paper. The authors operated under the assumptions of the aerobic capacity model for the evolution of automatic endothermy.
It is here that we come to the crux of the problem, and the main subject of this post.
This post took a little longer to get together than I expected. Much like the first installment of this series, I found myself writing more and more. This time, though, rather than bother with breaking the post up into a bunch of smaller sections, I’ve decided to just dump the whole thing online at once.
Don’t worry, I’ve provided lots of pretty pictures to ease the eye strain. 🙂
While an in-depth look at Tianyulong confiusci‘s filaments (or as in-depth as one can get with just photos), has left me with doubts regarding their validity, one question still lingers.
If the filaments do prove to be genuine epidermal structures, then what does this mean for dinosaurs in general?
When this little ornithischian was announced, many in the paleo community (in particular the paleo-art community) seem to have used this little guy as a license to draw feathers on pretty much any dinosaur. After all, if protofeathers are found in ornithischians and saurischians, then it seems likely that they were a basal trait for dinosaurs in general. Some have even argued that the filaments alleged for Tianyulong, along with the protofeathers of maniraptorans, and the “fur” in pterosaurs, are all homologous structures; thus making a “furry” covering a primitive (plesiomorphic) trait for all of Dinosauria.
This is where we really need to start putting the brakes on. One only needs to do a cursory examination of any archosaur cladogram to see that there is a problem with this argument.
Though it is all too often forgotten, we have found the skin impressions from practically every major dinosaur group known to science. You know what these impressions show?
In practically every case, “skin” impressions from dinosaurs show them to have been scaly. Impressions from hadrosaurs (Sternberg, 1909, Anderson et al 1999), ceratopians (Brown 1917, Sternberg 1925), stegosaurs (Xing et al 2008, and photo on the left), ankylosaurs (Parks, 1924), sauropods – including embryos (Coria and Chiappe 2007), and most theropods (Abelisaurs [Czerkas & Czerkas 1997], Allosaurs [Pinegar et al 2003] and Tyrannosaurs [Currie et al 2003]) have all shown the presence of hexagonal, or tuberculate scales. Dinosaurs were a decidedly scaly bunch. (Proto)feathers were the exception, not the rule.
A common counter-argument to this has been that protofeathers could have been lost as animals got larger, or that protofeathers were an ontogenetic thing, with fuzzy babies going bald as they reached adulthood.
The essential problem with this argument is that scales are not equivalent to naked skin.
Scales, like hair and feathers, are a form of integument. Though they form as an infolding of the epidermis, they nonetheless lie on top of it. There are certain mutations in reptiles that will produce scaleless mutants (e.g. “silkback” dragons). These mutants retain their epidermis (which often looks very loose). The epidermis can also be clearly viewed between the scales of snakes while they are swallowing a large prey item. If dinosaurs really did lose protofeathers as they got larger, then one would expect to see patches of naked skin in between patchy feathers (much like what we see in extant pachyderms), but that’s not what we are seeing.
It is often pointed out that birds have both scales and feathers, thus making it possible for scales to occur in conjunction with feathers on dinosaurs.
However, this generalizes the relationship between scales and feathers. The fact is scales in birds do not occur because of an absence of feathers, but rather from active suppression of feather formation (Sawyer and Knapp, 2003). If one has ever plucked a chicken one might notice a distinct lack of scales on the most of the body. Despite the fact that feathers form along tracts in the skin, the areas between these tracts remain bare. Ostriches (Struthio camelus) provide another prime example of this.
Ostriches are large birds that, like most large animals living in tropical climates, have undergone a fair amount of insulation loss in order to avoid overheating. One need only look at the bare flanks, or neck of an ostrich to see that scales are nowhere to be found on these section. Scales only occur on the tarsometatarsal (ankle and toe) portion of the body. In fact there is a rather sharp demarcation where this occurs. This demarcation agrees well with embryonic studies of diapsids which show how integument formation occurs (Alibardi & Thompson 2001).
Feather ÃŸ-keratin proteins are likely homologous with scale ÃŸ-keratin. However they are also smaller than scale proteins (likely caused by a deletion to the scale ÃŸ- keratin gene [Gregg et al 1984]). Taken together all of this suggests an antagonistic relationship between scales and feathers. One that would determine integument placement based off of where one protein cascade ends, and another one begins.
To put it another way, the chances of a scaly dinosaur with a feathery mohawk, are extremely unlikely.
The ontogenetic argument seems even less likely, as it posits that dinosaurs lost one type of integument as hatchlings and then grew a completely different type as they reached adulthood. This would make dinosaurs unique among vertebrates in doing that.
To summarize then, scaly dinosaurs were not “naked” like elephants and rhinos. If we are to believe that a dinosaur group lost protofeathers as it evolved to be larger, then we must also assume that group then re-evolved scales in its place.
It is at this point where a cladogram comes in handy.
The following are three cladograms showing the possible evolution of filamentous integument in archosaurs. Each terminal group is one that we know the integument for (though not the exact member who’s picture I used). I’ve simplified things a bit with the coelurosaurs due to the nebulous nature of both Sinosauropteryx prima and the putative tyrannosauroid Dilong paradoxus. This should have little effect on the results as all these guys would do is add even more steps to the following situations. The general outcome remains unchanged.
The following are a few hypotheses that have been proposed over the last month for dinosaur integument evolution.
Hypothesis 1: The filaments seen in Tianyulong, Psittacosaurus, maniraptors, and pterosaurs are all homologous structures, thus making protofeathers the plesiomorphic trait for all of Dinosauria.
Take a look at our first cladogram. The blue dots indicate cases where a trait was lost, or reversed. In order for our first hypothesis to be true, then protofeathers would have to have been lost a total of 7 times! Also keep in mind what I mentioned previously. We are not just talking about protofeather loss, but also scale re-acquisition. That would also have to have occurred 7 times; making for a whopping 14 evolutionary steps!
Hypothesis 2: The filaments seen in Tianyulong, Psittacosaurus, maniraptors, and pterosaurs are merely analogous to each other. They represent yet another case of convergent evolution.
As the second cladogram shows; if this position is true, then protofeathers would have evolved a total of 4 different times. Once in the theropod line, once in pterosaurs, and twice in Ornithischians. That’s still a lot, but not nearly as many as in our first case.
Hypothesis 3: Protofeathers were the plesiomorphic trait for ornithodirans (pterosaurs and dinosaurs), but were lost at the base of Dinosauria, and subsequently reacquired by various dinosaur groups over time.
As one can see from cladogram 3 there, this situation results in a messy outcome. We see a single re-evolution in theropods, while Ornithischians show a helter-skelter pattern of filament reacquisition, and subsequent loss. The result is 1 case of evolution, 4 cases of filament loss as well as 4 cases of scale reversal, and 2 cases of filament re-evolution; making for a grand total of 11 steps.
Technically one could make the 3rd cladogram a bit different by having filamentous integument evolve twice within Ornithischia. This reduces the steps needed to 6, and makes for a cladogram very similar to cladogram 2.
A general rule of thumb for systematic paleontology, is to assume that evolution takes the least amount of steps possible (we assume Nature is generally lazy that way). As such, the evolutionary situation that produces the fewest “steps” is assumed to be the most likely situation. Nature doesn’t have to flow that way. There are cases out there where evolution might take a more complicated road, but in general this assumption that the simplest explanation is the most likely, tends to hold up.
So what does that say about our current situation?
Assuming that filamentous integument occurred a few times in ornithodiran evolution, results in a cladogram with substantially fewer steps (4). As such, it appears the most likely, or most parsimonious case.
Protofeathery integument could still be basal to Dinosaurs, and all those necessary reversals could still have occurred, but the road getting there seems unnecessarily complicated, and thus rather unlikely.
As it stands right now, it appears that if the filaments on Psittacosaurus and Tianyulong did belong to their respective owners, then they are a case of convergent evolution. Though generally frowned upon in systematics (mostly because it is a pain in the ass for phylogenetics), convergence is a rather common feature of evolution. For instance, in squamates alone the evolution of live birth has occurred a conservative 100 times (Shine 2005)!
So yeah, convergence happens; even for seemingly complicated things. That the filaments in these ornithischians, bear almost zero similarity to those of Sinosauropteryx and kin, further supports the hypothesis that they are an independent case of evolution.
There is another alternative that seems to rarely get mentioned. It is possibile that these filaments are actually scale derivatives. This would not be that surprising. Scales produce a wide variety of different ornamental structures in extant reptiles (from strange nose protuberances in certain iguanians, to flashy frills in agamids, and soft velvety skin in some geckos). In fact, the presence of the Psittacosaurus “quills” alongside scales, suggest that they are more likely to be a scaly derivative, than a feathery one.
Gonocephalus grandis, Rhacodactylus ciliatus, and Atheris hispida. Just some examples of scale diversity in extant reptiles.
What of the other major implication for basal “fuzz” in dinosaurs. Does this clinch the “dinosaurs were warm-blooded” argument?
Despite the wishes of some of the more vocal dino enthusiasts on the internet, this does not signal the death knell for bradymetabolic dinosaurs.
Both mammals and birds have an insulatory coat. From what we can gather, the role (or one of the roles) of this coat is to keep body temperature fairly constant. Therefore it is tempting to look at both feathery birds and fuzzy mammals and assume that a high metabolic rate (or automatic endothermy) must be associated with insulation.
However mammals and birds only represent two instances of insulation. As any statistician will tell you, two points make a line, not a pattern. What would help would be if there was at least one other group of critters that had insulation.
Well, it turns out that there are: Arthropods.
From the “woolly crustaceans” of the deep ocean, to bees and tarantulas, “hair” is fairly common among arthropods. This hair (deemed: setae) has a different embryological origin from mammalian hair, so it cannot be considered homologous.
So there is a third outgroup that shows filamentous coverings. Is it also associated with a constant body temperature and automatic endothermy?
In many species, the setae appear to function primarily as touch sensors; whether it be for the legs of a fly, or the body of a orb weaving spider. Still there are a few (moths, bees, certain beetles), that do use their hair for insulation. These animals are “functional endotherms.” That is to say that they use muscular power to generate heat internally. The difference between them and the classic “warm-blooded” mammals and birds, is that heat is generated solely by “skeletal” muscle, and can be turned off.
That insulation should not automatically equal “warm-bloodedness” has been recognized before. Previous authors (Schmidt-Nielson 1975, Withers 1992) have pointed out that while insulation does seem to lead to homeothermy, it does not associate so well with a high metabolism.
So then could we say that Tianyulong and the “feathered” theropods were using their insulation to maintain a stable body temperature.
If one is to use filaments for insulation, then they need to be spaced close enough that they will trap a layer of air between them and the skin. In mammals and birds this results in a notably fuzzy coat. Yet, sometimes this look can be deceiving. Consider polar bears. Despite their hairy look, polar bear fur offers very little insulatory benefits (Lavers 2000). The main use for the fur, seems to be to hide the black, sun absorbing skin underneath. Polar bears stay warm by maintaining a large layer of fat between their skin and the body core. The wide spacing of the hairs also allows them to quickly drain water from the body when the bears emerge from their icy swims (where insulation benefits of fur equal exactly zero). So if one is going to keep warm by being fuzzy, then that fuzz better be pretty thick.
For the protofeathered/feathered maniraptorans, the fuzz count appears high enough to allow for functional (possibly passive) homeothermy. This is not the case with Tianyulong. The filaments in T.confiusci are spaced too far apart to allow for much in the way of heat retention. These filaments must have been used for something else. Possibly as a means of defense by keeping attention focused on the tail, or (if backed by erector muscles) by making the animal look substantially bigger and more intimidating to a potential predator. They may have been used in a more passive sense by conferring camouflage to their owner. All are possible alternative uses for these filaments (ignoring, for now, the likelihood of these filaments being used for multiple purposes).
Besides all that, the Mesozoic is well known for being a time of high global temperatures. This doesn’t lend well to the assumption that filaments were evolved to keep their owners warm.
Now if they evolved to help keep heat out…
Anderson, B.G., Barrick, R.E., Droser, M.L., Stadtman, K.L. 1999. Hadrosaur Skin Impressions fom the Upper Cretaceous Neslen Formation, Book Cliffs, Utah: Morphology and Paleoenvironmental Context. Vertebrate Paleontology in Utah. David Gillette (ed). Utah Geo Survery. ISBN: 1557916349, 9781557916341 pps: 295-302.
Alibardi, L. and Thompson, M. 2001. Fine Structure of the Developing Epidermis in the Embryo of the American Alligator (Alligator mississippiensis, Crocodilia, Reptilia). J. Anat. Vol.198:265-282.
Brown, B. 1917. A Complete Skeleton of the Horned Dinosaur Monoclonius and Description of a Second Skeleton Showing Skin Impressions. Bul AMNH. Vol.37(10):281-306.
Coria, R.A. and Chiappe, L.M. 2007. Embryonic skin from Late Cretaceous Sauropods (Dinosauria) of Auca Mahuevo, Patagonia, Argentina. J. Paleo. Vol.81(6):1528-1532.
Currie, P.J., Badamgarav, D., Koppelhu, E.B. 2003. The First Late Cretaceous Footprints from the Nemegt Locality in the Gobi of Mongolia. Ichnos. Vol.10:1-12.
Czerkas, S. A., and S. J. Czerkas. 1997. The integument and life restoration of Carnotaurus. In D. L. Wolberg and G. D. Rosenberg (eds.), Dinofest International, Proceedings of the Symposium at Arizona State University, pp. 155?158. Philadelphia Academy of Natural Sciences, Philadelphia.
Gregg, K., Wilton, S.D., Parry, D.A., and Rogers, G.E. 1984. A Comparison of Genomic Coding Sequences for Feather and Scale Keratins: Structural and Evolutionary Implications. Embo J. Vol.3(1): 175-178.
Lavers, C. 2000. Why Elephants Have Big Ears: Understanding Pattersn of Life on Earth. St. Martins Press. NY. ISBN: 0312269022. pg 104.
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Sternberg, CM., 1925, Integument of Chasmosaurus belli: Canadian Field Naturalist, v.39, p. 108-110.
Given all the recent stink over a certain other documentary, I’m not exactly itching to jump back into dino docs.
The Public Broadcasting Service’s long running series NOVA, has a new episode out, entitled Arctic Dinosaurs. The episode is about a particularly exciting find in Alaska, and its implications for our view on dinosaurs. The researchers; namely museum Victoria’s Tom Rich and MNS Dallas’ Anthony Fiorillo, came across a fossil bed along Alaska’s north slope, that revealed the existence of hadrosaurs, ceratopians and coelurosaur theropods, all living in far North Alaska.
As I had mentioned previously, NOVA tends to get lauded for its well put together documentaries. I would argue that this doc was no different; though there were some missteps that I feel may be a sign of NOVA’s producers trying to fall more in line with the fare seen on Discovery Channel and the A&E networks.
Secondly, I would like to lambast PBS for what is probably their most egregious error with this, and other NOVA specials. Namely the lack of Firefox love. The only way I am able to watch these NOVA specials is by firing up Internet Explorer. If I use Firefox all that happens is I get a dead loading screen.
The premise of the series is fine, and as in previous iterations, NOVA has done a good job of letting the scientists talk how scientists really talk (i.e. with lots of caution and caveats).
I was far less impressed with the writing for the narrator. There were more than a few instances where the narrator resorted to straight up hyperbole. Especially in the beginning when it is revealed that all these dinosaur fossils had been found in this polar state.
The narrator said:
The startling discovery that these ancient reptiles, “thunder lizards,” lived and thrived in the arctic has taken scientists by surprise.
Then a little later:
According to conventional wisdom, it shouldn’t be here, because this is how dinosaurs are typically pictured: cold-blooded reptiles living in tropical climes, not in cold, arctic environments like this one. And the Hadrosaur is not alone.
Um, no. We have had discoveries of dinosaurs, and other reptiles from polar and paleo-polar latitudes, for decades now. The real neat thing about this find, was the sheer number of animals discovered. This doc served more as a review of what we have learned so far, rather than a breaking news story.
There was another writing snafu that occurred a little further in too that I feel needs clarifying:
Scientists long believed that dinosaur biology resembled that of cold-blooded reptiles like crocodiles, animals that require warmth to survive and cannot withstand prolonged exposure to temperatures below freezing. But not one crocodile fossil has been found along the Colville, which suggests that polar dinosaurs found a way to adapt to an environment that their cold-blooded cousins couldn’t tolerate. But how?
This statement is misleading. We do have evidence of non-dinosaurian polar reptiles. These include Cretaceous crocodylian and turtle fossils found in Victoria, Australia (which would have been closer to the South Pole) and Axel Heiberg Island in Canada, as well as plesiosaur fossils from Antarctica, and at least the assumption that Meiolaniid turtles (large, ankylosaur like armoured turtles that lived from the late Cretaceous through to the Pleistocene) had once lived in Antarctica.
Oh, and also Leaellynasaura amicagraphica was a herbivore; not a carnivore as was stated in the show.
So there were those few writing missteps. The only other thing I can fault the show for was its very lackluster CG work. As NOVA is a mostly public funded series, I can forgive the lower quality CG work, though I still think they could have afforded to make their models at least a tad more realistic (especially since they teased feathers on Dromaeosaurus albertensis before returning to scaly maniraptors (i.e. the Troodon formosus). Plus their Gorgosaurus libratus was just atrocious.
Regardless, most of these complaints are small. The writing flubs were probably the worst offenders. Short of that, the show was well put together. Though the show still fell a little more in the pro-warm-blooded camp for dino metabolism, it was the first and only time I have ever heard a documentary point out that warm-blooded and cold-blooded are opposite ends of a continuum. In fact one of the better writing moments occurred towards the end when the narrator stated:
Dinosaurs likely had their own unique solution to the body temperature problem, which allowed them to survive for millions of years in the toughest seasonal conditions their world had to offer.
It was nice to see a documentary that actually took a more objective stance on the whole thermophysiological debate.
Finally another big plus for this show was the sheer number of paleontologists that rarely seem to make it in front of the camera, including Hans-Dieter Sues and Anusuya Chinsamy-Turan (the latter of whom while being a great scientist, has one of the harder to pronounce names in paleontology).
Overall, this was another fine piece of work from the folks over at NOVA. Though there was a tendency to stray into the realm of hyperbole with the narration, and the CG work is somewhat painful to watch, the show proved informative and interesting.
In the end, that’s really all a documentary should strive for.
Actually, I’ve never thought that sauropods were grey. Mammals in general tend to be rather bland in their colour schemes. Reptiles don’t have that problem. With xanthaphores (yellow pigmented cells), erythrophores (red pigmented cells) iridophores (iridescent cells) and melanophores (dark pigmented cells), the range of colour available to reptiles, and by extension – dinosaurs, is quite vast.
That said, I always pictured sauropods as either a brownish green colour, or maybe a very pale blue (blue is generally rare in tetrapods, hence the thought of it being a weak blue).
But I digress.
I grew up during an interesting time for dinosaur research. Unlike the majority of paleontologists working right now I didn’t grow up learning about dinosaurs being slow and sluggish mistakes of nature. I also didn’t grow up with the “hummingbirds on crack” version of dinosaurs that is currently pervading popular culture. Rather, I grew up during that strange transitory phase of the Dinosaur Renaissance where dinosaurs were sometimes viewed as sluggish beasts and other times as racecars of the Mesozoic.
The result, I think, has been a slightly detached and objective look at how perceptions of dinosaurs have changed over time.
A “Brontosaurus” getting attacked by Allosaurus during a sojourn on land to lay her eggs. Ah, the classics.
One book I remember fondly was the Golden Book of Dinosaurs (shown above). It featured these beautiful drawings of dinosaurs living life as best we thought at the time. One picture that really stuck in my head, was a shot of two Brachiosaurus; one on land and the other so deep in a lake that one could only make out the crest on the head. I found that page to be so immersive and atmospheric. My knowledge of physics was not so good at the time, so it never dawned on me that this poor sauropod was basically breathing through a straw with its lungs separated by at least 2 atmospheres from the air entering (as best it could) the nostrils.
Then around the early nineties when Jurassic Park the book came out I started to note a distinct change in how dinosaurs were being portrayed. No longer were sauropods swamp bound behemoths. Now they were fully terrestrial titans that could not only support their weight on all four legs, but could even do so on 2 (well 3 if one counts the tail). It was around this time that Robert Bakker’s infamous “Dinosaur Heresies” started making the rounds.
Now, admittedly, Heresies came out in 1986 and the changing view of dinosaurs actually started in the seventies. However, it wasn’t until the early nineties that the full effects of Bakker’s work could truly be appreciated. If anything this gives one an idea of the kind of inertia one must deal when it comes to getting scientific ideas out into the public.
Again I digress.
It was around the early nineties when I first read The Dinosaur Heresies. The first few chapters were amazing. I had never seen dinosaurs portrayed this way. They walked better and were more active. In many ways they better fit the concept I had in my head all along.
Then I came up to the end of chapter 3. The thesis of this chapter was to explain why reptiles should not be viewed as inferior to mammals. In order to do so Bakker explained all the various ways in which extant reptiles outshine extant mammals. The end of the chapter features a beautifully drawn shot of the “panzer croc” Pristichampsus snatching a Hyracotherium (formerly Eohippus). The caption read:
Pristichampsus hunted during the Eocene Epoch, about 49 million years ago, but it was very rare, much rarer than big mammalian predators, proof that cold-bloodedness was a great disadvantage.
That’s when the real thesis of the book hit me. The argument wasn’t: “Dinosaurs weren’t slow and stupid, because of the following.”
Rather the argument was: “Dinosaurs weren’t cold-blooded because the facts show the following.”
In order to pull dinosaurs out of the mire, Bakker had to change their fundamental thermophysiology. The general concept, that cold-bloodedness is inferior to warm-bloodedness, remained the same. This despite Bakker’s initial attempt to explain how “cold-blooded” reptiles outshine “warm-blooded” mammals.
Bakker’s book was just the start. From there, we had Adrian Desmond’s “The Hot Blooded Dinosaurs” (okay, technically Desmond was first by 7 years, but he largely stole Bakker’s work to make the book so it evens out) and Gregory S. Paul’s infamous: “Predatory Dinosaurs of the World.” Each new book taking the “dinosaurs can’t be cold-blooded” argument a little further. By the time we hit Predatory Dinosaurs of the World, Tyrannosaurus rex was running along at 40mph, dromaeosaurs were practically flapping around and every species of dinosaur was reaching adult size by between 4-10 years of age.
Sadly it was at this point that Jurassic Park was written. As hardcore fans know it was Greg Paul’s erroneous sinking of Deinonychus antirrhopus into Velociraptor that gave us the JP “raptors.” It was also at this point that the pendulum of dinosaur physiology officially swung the other way.
The thing that had always bugged me about this view of dinosaurs was the sheer lack of supporting data for it. The assumption was always that dinosaurs were so vastly different from “typical reptiles” that they had to have been doing something different. Yet when one looked at the actual data dinosaurs came out looking slightly odd at best. For the most part dinosaurs fit the reptile mold quite well. It was these elusive “classic reptiles” that didn’t appear to exist.
Most reptiles don’t fit the “typical reptile” mold at all. Yet despite numerous papers over the past 30 years depicting reptiles doing things normally thought un-reptile like (e.g. caring for their young, competing with large mammals, etc), most of this was dutifully ignored in favour of an older, more outdated view.
It was a problem that Nicholas Hotton III (1980) aptly called: The “endothermocentric fallacy.” Basically, the assumption that being an endotherm is inherently superior to being an ectotherm. Part of that superiority included the ability of endotherms to do everything faster and “better” than similar sized ectotherms. This problems with this way of thinking warrants an entire blog post to itself. So rather than get bogged down with this particular I’ll touch more on the endothermocentric fallacy at a later date. For now all that one needs to keep in mind is that the thinking of the time was that if dinosaurs were going to be active at all then they had to be endotherms.
By the late nineties we had the first evidence of feathers in a small branch of the theropods (Maniraptora). Birds were officially adopted into the dinosaur family tree and the fully endothermic concept of Dinosauria was completely entrenched.
The funny thing, of course, is that this dogmatic view of dinosaur metabolism was just as bad as the early 20th century’s “cold-blooded” swamp bound view. Sure dinosaurs were more active now, but the data supporting it was just as nebulous as the stuff that was used to keep dinos in the swamp.
Enter the 21st century, and the late…um, 0’s (does anyone have a name for this decade yet?). Biomechanic work on dinosaurs has started to reveal amazing insights into the physical limits of what dinosaurs could do, and the results have started to pull the pendulum back again.
Work by John Hutchinson and Mariano Garcia (2002) on T. rex showed that not only could T. rex not hit 40mph, but it technically couldn’t run either. A biomechanical assessment of theropod forelimbs by Ken Carpenter (2002) has shown that the “bird-like” dromaeosaurs could not fold their arms up like birds after all.
Work by Rothschild and Molnar (2005) on sauropod stress fractures showed no signs of rearing activity in sauropods, while work by Kent Stevens and J. Michael Parrish (2005) pulled the swan-like curve out of sauropod necks, placing things far more horizontally.
Work by Gregory Erickson and others (2001) on micro-slices of dinosaur bone has indicated that very few dinosaurs hit adult size in less than 15 years.
Now we have a new study by Lehman and Woodward (2008) which follows up on Erickson et al’s work and actually shows that even this toned down version of dinosaur growth is probably too fast as well. Lehman and Woodward focused on sauropods and studies on their bone microstructure. What they did was compare bone growth data to a well used equation for growth in animals.
Deemed the Bertalanffy equation; it states that the mass at any given age is an exponential function limited by the asymptote of adult body mass. This equation has been used extensively in studies on bird and elephant growth among others. An example of the equation is given to the right for fish.
When the authors did this they discovered something quite interesting. Instead of taking 15 years to reach adult mass, sauropods like Apatosaurus excelsus took closer to 70 years!!
Other sauropods measured took between 40 and 80 years! This is a substantial decrease in growth rate estimated before. Mind you this is data taken, in some cases, from the same piece of bone that Erickson et al had used. So one can’t suggest anomalous bones being used as the reason behind the surprising results. The authors also went to great lengths to take into account differences in mass estimations as well as allometric growth of body parts. In each case the changes had little affect on the overall outcome (in many cases, it made growth go even slower).
Now keep in mind we are talking about the time it took sauropods to reach full adult size. This is not the time taken to reach sexual maturity. Earlier studies by Erickson et al (2007) had already discovered that dinosaurs didn’t wait to grow up before engaging in sex, so there is no issue here of 80 year old sauropods finally “doing the nasty.”
What this does show is that growth in dinosaurs might not be as determinate as initially thought. An 80 year old sauropod might just have been close to the edge of its lifespan at this point (though the possibility of bicentennial sauropods does still exist). It also shows that dinosaurs had growth rates far closer to the realm of reality (before it was hard to imagine how an Apatosaurus excelsus was able to pound down enough food daily to add 13.6 kg of new mass a day. Especially given their small mouths).
Thermophysiologically what does this all mean? Were dinosaurs “cold-blooded” after all?
That’s one of those questions that will never be fully answered (short of a time machine). What this does do is pull dinosaurs ever further away from the “definitely warm-blooded” category and push them right back into the middle again. When/if the dust settles on this metabolism debate I suspect that dinosaurs will probably remain in the middle somewhere.
Of course while all of this is going on with dinosaurs we have other studies, like those from Tumarkin-Deratzian (2007) showing the existence of fibrolamellar bone growth in wild alligators, that are finally moving the rusty pendulum of reptile metabolism out of the “classic reptile” category and much closer to the middle.
So in the end dinosaurs will still probably wind up being “good reptiles.” Thankfully the exact definition of what that entails will have probably changed by then.
Bakker, R. 1986. The Dinosaur Heresies: New Theories Unlocking the Mystery of the Dinosaurs and their Extinction. William Morrow. New York.
Carpenter, K. 2002. Forelimb Biomechanics of Nonavian Theropod Dinosaurs in Predation. Concepts of Functional Engineering and Constructional Morphology. Vol. 82(1): 59-76.
Desmond, A. 1976. The Hot Blooded Dinosaurs: A Revolution in Paleontology. Dial Press.
Erickson, G.M., Curry Rogers, K., Varricchio, D.J., Norell, M.A., Xu, X. 2007. Growth Patterns in Brooding Dinosaurs Reveals the Timing of Sexual Maturity in Non-Avian Dinosaurs and Genesis of the Avian Condition. Biology Letters Published Online. doi: 10.1098/rsbl.2007.0254
Erickson, G.M., K. C. Rogers, and S.A. Yerby. 2001. Dinosaurian Growth Patterns and Rapid Avian Growth Rates. Nature 412: 429?433.
Hotton, N., III. 1980. An Alternative to Dinosaur Endothermy: The Happy Wanderers. In A Cold Look at the Warm-Blooded Dinosaurs (R.D.K. Thomas and E.C. Olson Eds.), pp. 311-350, AAAS, Washington, DC
Hutchinson, J.R., Garcia, M. 2002. Tyrannosaurus was not a fast runner. Nature 415: 1018-1021.
Lehman, T.M., and Woodward, H.N. 2008. Modeling Growth Rates for Sauropod Dinosaurs. Paleobiology. Vol. 34(2): 264-281.
Rothschild, B.M., and Molnar, R.E. 2005. Sauropod Stress Fractures as Clues to Activity. In Thunder Lizards: The Sauropodomorph Dinosaurs. (Virginia Tidwell and Kenneth Carpenter eds). Indiana University Press. pp 381-394.
Stevens, K.A., and Parrish, J.M. 2005. neck Posture, Dentition, and Feeding Strategies in Jurassic Sauropod Dinosaurs. In In Thunder Lizards: The Sauropodomorph Dinosaurs. (Virginia Tidwell and Kenneth Carpenter eds). Indiana University Press. pp 212-232.
Tumarkin-Deratzian, A.R. 2007. Fibrolamellar bone in adult Alligator mississippiensis. Journal of Herpetology. Vol. 41. No.2:341-345.